The nucleoid-associated proteins H-NS and FIS modulate the DNA supercoiling response of the pel genes, the major virulence factors in the plant pathogen bacterium Dickeya dadantii

Abstract

Dickeya dadantii is a pathogen infecting a wide range of plant species. Soft rot, the visible symptom, is mainly due to the production of pectate lyases (Pels) that can destroy the plant cell walls. Previously we found that the pel gene expression is modulated by H-NS and FIS, two nucleoid-associated proteins (NAPs) modulating the DNA topology. Here, we show that relaxation of the DNA in growing D. dadantii cells decreases the expression of pel genes. Deletion of fis aggravates, whereas that of hns alleviates the negative impact of DNA relaxation on pel expression. We further show that H-NS and FIS directly bind the pelE promoter and that the response of D. dadantii pel genes to stresses that induce DNA relaxation is modulated, although to different extents, by H-NS and FIS. We infer that FIS acts as a repressor buffering the negative impact of DNA relaxation on pel gene transcription, whereas H-NS fine-tunes the response of virulence genes precluding their expression under suboptimal conditions of supercoiling. This novel dependence of H-NS effect on DNA topology expands our understanding of the role of NAPs in regulating the global bacterial gene expression and bacterial pathogenicity.

Interplay of digital and analog control in time-resolved gene expression profiles

“…Previous findings that the vegetative RNAPσ 70 and the stationary phase RNAPσ S holoenzymes cooperate with different sets of transcription factors [3] are fully consistent with this notion. Moreover, activation of RNAPσ S holoenzyme on transition to stationary phase is associated with DNA relaxation and expression of other abundant NAPs such as IHF, Lrp and Dps followed by morphological reorganisation of the nucleoid and activation of communications between the chromosomal arms in the replication terminus [26,39,43], again in keeping with the second peak of analog CTC observed in our study.…”

“…The results of a wide range of our own investigations over the last years have their foundations in statistical physics and information theory [2,4,[25][26][27][28][29][30][31]. They have cemented the notion of a tight interplay of the regulatory network implemented via TFs and their binding sites (digital control); and the regulation implemented via alterations of chromosomal configuration and DNA compaction (analog control) in bacterial gene regulation (depicted in Fig.…”

The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity

“…In vivo, two principal functions have been ascribed to H-NS: as a repressor of certain genes and gene clusters located in A/T-rich regions of the genome (Navarre et al 2006;Ouafa et al 2012), and as a domainin, assumed to function by stabilizing barriers between distinct topological domains (Hardy and Cozzarelli 2005). Both functions are compatible with the structures assumed by plectonemically coiled DNA superhelices.…”

Unravelling the Role of the F55 Regulator in the Transition from Lysogeny to UV Induction of Sulfolobus Spindle-Shaped Virus 1

“…This architecture strongly resembles that of the nonlambdoid UV-inducible coliphage 186 (35,36), although a different mechanism may be evoked. Indeed, it has been proved in both eukaryotes (37)(38)(39) and prokaryotes (40)(41)(42) that transcription of genes separated by a few kilobases is not independent but is coupled by torsional stress, which, by influencing the opening properties of the promoters, facilitates or hinders transcription initiation. This kind of influence reduces the expression of convergent gene couples (43), such as in the case of T lys and T ind .…”